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Abstract

Background. The turtle body plan differs markedly from that of other vertebrates and serves as a model system for studying structural and developmental evolution. Incorporation of the ribs into the iconic turtle shell negates the rib movements that effect lung ventilation in the majority of air-breathing amniotes (the clade encompassing mammals, lizards, turtles, birds, and crocodilians). Instead, turtles have a novel abdominal-muscle-based ventilatory apparatus whose evolutionary origin remains a mystery. Methods. Here we show through broadly comparative anatomical and histological analyses that the earliest stem-group turtle form the middle Permian (260 mya), Eunotosaurus africanus, has several turtle-specific lung ventilation characters: rigid ribcage, inferred loss of intercostal muscles which drive costal ventilation in all other amniotes, and histological correlates for the primary muscle, M. transverses, used in exhalation. Results. Our results place the origin of the unique lung ventilatory apparatus of extant turtles shortly after the divergence of turtles from other reptiles and approximately 50 million years before the oldest known fully developed shell. Discussion. These data indicate that it was an easing of structural constraints through division of function (divergent specialization) between the ribs and abdominal musculature that facilitated the evolution of both the novel turtle lung ventilation mechanism and the turtle shell.

Author Comment

This is an abstract that has been accepted in Nature Communications (DOI: 10.1038/ncomms6211) and for the 5th Turtle Evolution Symposium.

Additional Information

Competing Interests

The authors declare that they have no competing interests.

Author Contributions

Tyler Lyson conceived and designed the experiments, performed the experiments, analyzed the data, contributed reagents/materials/analysis tools, wrote the paper, prepared figures and/or tables, reviewed drafts of the paper.

Jennifer Botha-Brink performed the experiments, analyzed the data, contributed reagents/materials/analysis tools, wrote the paper, reviewed drafts of the paper.

Torsten Scheyer performed the experiments, analyzed the data, contributed reagents/materials/analysis tools, wrote the paper, prepared figures and/or tables, reviewed drafts of the paper.

Markus Lambertz performed the experiments, analyzed the data, contributed reagents/materials/analysis tools, wrote the paper, prepared figures and/or tables, reviewed drafts of the paper.

Gaberiel Bever analyzed the data, wrote the paper, reviewed drafts of the paper.

Bruce Rubidge analyzed the data, contributed reagents/materials/analysis tools, wrote the paper, reviewed drafts of the paper.

Kevin de Queiroz analyzed the data, contributed reagents/materials/analysis tools, wrote the paper, reviewed drafts of the paper.

Funding

Funding was provided by a NMNH Peter Buck postdoctoral fellow to TRL, a NSF grant to C. Farmer (IOS 1055080) to help support ERS, the Palaeontological Scientific Trust (PAST) and its Scatterlings of Africa programmes and the National Research Foundation funding to JBB (UID 82584), the NRF and DST\NRF Centre of Excellence in Palaeosciences, and Palaeontological Scientific Trust (PAST) and its Scatterlings of Africa programmes to BSR, and a Swiss National Science foundation grant to TMS (31003A 149506). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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